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Sensory input arrives from thalamus in cortical layer (L) 4, which outputs predominantly to superficial layers. L4 to L2 thus constitutes one of the earliest cortical feedforward networks. Despite extensive study, the transformation performed by this network remains poorly understood. We use two-photon calcium imaging to record neural activity in L2-4 of primary vibrissal somatosensory cortex (vS1) as mice perform an object localization task with two whiskers. Touch responses sparsen and become more reliable from L4 to L2, with nearly half of the superficial touch response confined to ~1 % of excitatory neurons. These highly responsive neurons have broad receptive fields and can more accurately decode stimulus features. They participate disproportionately in ensembles, small subnetworks with elevated pairwise correlations. Thus, from L4 to L2, cortex transitions from distributed probabilistic coding to sparse and robust ensemble-based coding, resulting in more efficient and accurate representations.

Primary sensory cortices display functional topography, suggesting that even small cortical volumes may underpin perception of specific stimuli. Traditional loss-of-function approaches have a relatively large radius of effect (>1 mm), and few studies track recovery following loss-of-function perturbations. Consequently, the behavioral necessity of smaller cortical volumes remains unclear. In the mouse primary vibrissal somatosensory cortex (vS1), “barrels” with a radius of ∼150 μm receive input predominantly from a single whisker, partitioning vS1 into a topographic map of well defined columns. Here, we train animals implanted with a cranial window over vS1 to perform single-whisker perceptual tasks. We then use high-power laser exposure centered on the barrel representing the spared whisker to produce lesions with a typical volume of one to two barrels. These columnar-scale lesions impair performance in an object location discrimination task for multiple days without disrupting vibrissal kinematics. Animals with degraded location discrimination performance can immediately perform a whisker touch detection task with high accuracy. Animals trained de novo on both simple and complex whisker touch detection tasks showed no permanent behavioral deficits following columnar-scale lesions. Thus, columnar-scale lesions permanently degrade performance in object location discrimination tasks.

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